Cent. Eur. J. Biol. • 9(1) • 2014 • 11-18 DOI: 10.2478/s11535-013-0120-6

Central European Journal of Biology

Enemy at the gates: introduction potential of non-indigenous freshwater in Greece via the aquarium trade

Research Article

Irene Papavlasopoulou1, Costas Perdikaris2,*, Leonidas Vardakas3, Ioannis Paschos4

1Department of Veterinary Medicine, University of Thessaly and Department of Aquaculture & Fisheries, Technological Educational Institute of Epirus, 43100 Karditsa, Greece

2Department of Fisheries, Regional Unit of Thesprotia, Region of Epirus, 46100 Igoumenitsa, Greece

3Institute of Inland Waters, Hellenic Centre for Marine Research, 19013 Anavissos, Greece

4Department of Aquaculture & Fisheries, Technological Educational Institute of Epirus, 46100 Igoumenitsa, Greece

Received 11 May 2012; Accepted 23 October 2012

Abstract: Indigenousfreshwater crayfish species (ICS) are important biodiversity components and desirable fishery targets. However,ICS populationsareincreasinglythreatenedbyvariousanthropogenicstressors.Moreover,establishedpopulationsofnon-indigenous freshwatercrayfishspecies(NICS)andnew‘waves’ofNICSintroductionsexertsignificantpressureonICSpopulationsatapan- Europeanlevel.Theseeffectsincludedirectcompetitionforspaceandresourcesaswellascrayfish‘plague’transmissionfrom introduced North American species. Given low public knowledge of this problematic, considerable risk of future introductions exist as a result of conventional and internet-based aquarium trade, which often lead to deliberate and/or accidental releases of NICS into the wild. In 2011, we conducted a survey of freshwater crayfish species in eleven large-size pet shops located in three major cities and in three large internet-based aquarium companies in Greece. Overall, eight species belonging to three genera (Procambarus, Cherax and ) were recorded, originating from the USA, Australia, New Guinea and Mexico. The invasion potential of the three most popular species was assessed using the Freshwater Invertebrate Invasiveness Scoring Kit (FI-ISK). Two species were determined to constitute a ‘very high risk’ of invasion. As such, regulatory measures need to be implemented to monitor the ornamental trade of NICS in Greece and a national framework developed for protecting ICS.

Keywords: Aquarium trade • Biodiversity • FI-ISK • Non-indigenous freshwater crayfish ©VersitaSp.zo.o.

1. Introduction eutrophication and overexploitation [1]. Furthermore, increasing information on NICS introductions into European Several populations of indigenous freshwater crayfish freshwaters [2] indicates a serious risk of extinction for species (ICS) in Europe are at risk of becoming local populations in the near future through both direct endangered or extinct as a result of various anthropogenic (e.g. predation and crayfish ‘plague’) and indirect effects stressors such as the crayfish ‘plague’ disease, other (e.g. grazing of aquatic macrophytes, alteration of diseases, competition with invasive non-indigenous biomass and species richness of macroinvertebrates, crayfish species (NICS), translocations of both ICS and bank erosion and substrate disturbance) [3]. The latter NICS, loss of genetic diversity, pollution, water abstraction could exert dramatic changes to the biodiversity of aquatic for irrigation and direct human use, habitat destruction, communities and the integrity of ecosystems in Europe.

* E-mail: [email protected] 11 Enemy at the gates: introduction potential of non-indigenous freshwater crayfish in Greece via the aquarium trade

Recent efforts to review and record historical and (FI-ISK) tool developed by the Centre for Environment current occurrences of ICS in Greece [4-6] showed Fisheries and Aquaculture Science (CEFAS) that crayfish populations are present in at least 34 (http://cefas.defra.gov.uk/our-science/ecosystems-and- hydrographic systems (natural and man-made lakes, biodiversity/non-native-species/decision-support-tools. rivers and small streams). However, the distribution aspx) to assess the invasion potential of the three most of crayfish is much more restricted nowadays than popular aquarium species (Procambarus clarkii, Cherax in previous decades, and many populations of ICS destructor and Cherax quadricarinatus). The same tool are isolated and confined to headwaters and lentic was also applied to ICS and NICS in Greek freshwaters environments that remain pristine [4]. Although there systems for comparison purposes. is only one established population of invasive NICS (i.e. signal crayfish Pacifastacus leniusculus (Dana, 1852)), ICS (noble crayfish Astacus astacus (L.), 3. Results narrowclawed crayfish Astacus leptodactylus Eschscholtz 1823, stone crayfish Austropotamobius Overall, we recorded eight species of NICS belonging torrentium (Schrank, 1803)) and their habitats are to three genera (Table 1). Available data for four species confronted to serious threats due to human-mediated (Procambarus clarkii, Cherax quardicarinatus, Cherax stressors. These threats are expected to be exacerbated peknyi and Cambarellus patzcuarensis) suggested that by globalization leading to increased trade and they were imported from Singapore. C. quardicarinatus e-commerce of NICS, unrestricted movement/travelling may also have been imported from an alternative of NICS, intense economic activity, demographic location in Italy. The species most advertised for sale in pressures [7,8] and climate change, which generally the e-commerce were P. clarkii and C. quadricarinatus. favour NICS with less strict ecological preferences and The FI-ISK revealed that invasion potential was increased adaptive ability compared to ICS [3]. Recently, particularly high for P. clarkii and C. destructor. The astacologists have determined that the aquarium trade analysis rejected these species for introduction in is as one of the most important and plausible sources of the aquarium trade based on a 16 points threshold. NICS introductions in Europe and worldwide. However C. quadricarinatus had moderate score, requiring data on the Hellenic aquarium trade of NICS is lacking. further assessment for introduction. The FI-ISK scores So far, aquatic ecologists have focused on studying are presented in Figure 1 against: (a) the scores for the and managing ecosystems already invaded and three ICS and the only NICS established in Greece; and degraded by non-indigenous species. Precautionary (b) the scores generated by Tricarico et al. [9] for the measures are urgently needed for mitigating further same species in Italy. Accurate scoring for C. peknyi, introductions of non-indigenous species, one of the P. alleni, C. shufeldtii, C. montezuma and most important threats to biodiversity worldwide. Here, C. patzcuarensis was not possible due to the limited our objective was to record the presence of ornamental bibliographic data on their biology and invasion ecology. NICS in the Greek aquarium trade market and assess their invasion potential into the wild. 4. Discussion

2. Experimental Procedures European ICS populations have suffered from serious declines during the last century, mainly due to the spread We recorded the presence of NICS in eleven large- of the crayfish ‘plague’ diseasevia introduced American size aquarium stores in Greece’s two largest cities species. All crayfish of Northern and Central American (Athens and Thessaloniki) and one large provincial origin, such as species from the genera Pacifastacus, city (Ioannina) between January and December 2011. Procambarus, Cambarellus and Orconectes are We also conducted an online-based research of three suspected vectors of crayfish ‘plague’. Freshwater major internet-based companies with stores in the crayfish are particularly good invaders compared to Greek pet market simultaneously. Data on the number other groups of aquatic organisms. Currently, ten of sales per store were not available. However, we NICS are established in the European freshwaters anecdotally recorded that nine specimens of the most with establishment success record approaching 100%, ornamental and large-size C. quardicarinatus were compared to the number of introduced species to the wild sold during 2011 in one store in the city of Ioannina [10]. Although NICS are still absent from neighbouring with a population of 100,000 inhabitants. We used the countries to Greece (i.e., Albania, the former Yugoslav Freshwater Invertebrate Invasiveness Scoring Kit, v1.19 Republic of Macedonia, Bulgaria, and Turkey) [2,5],

12 I. Papavlasopoulou et al. [ 27 ] Source [ 3 , 9 20 ] [ 3 , 20 25 26 ] [ 3 , 9 20 25 26 ] Documented/ possible impacts Unknown but a variety of pathogens is associated with the species. Rapid growth could be an advantage over the ICS in warm-water conditions. Invasive. Impacts in the area of origin (altering the cycling of nutrients and the structure of the food webs, competition with other endemic freshwater crayfish species, possible carrier of pathogens), but not yet documented in Europe. It is expected to become a major threat to ICS ( i.e. outcompete and displace them due to tolerance of environmental fluctuations, rapid growth and reproductive advantages). Very highly invasive ability, highly invasive ability, Very carrier of the ‘plague’, competition with ICS for space and resources, structural changes in food webs, predation, bioaccumulation, elimination/reduction of abundance and richness of indigenous species, damages to agricultural crops, ditches and river banks, increased water turbidity. Unknown but possible carrier of the ‘plague’. Habitat preferences Primarily lotic (rivers and water holes). Lentic-Lotic (slow-moving water with heavy vegetation,ponds, ditches and swamps, streams, rivers). Lentic (stagnant waters, pools and flooded marshes). Lentic including saline waters (swamps, marshes seasonally flooded wetlands, slow flowing water, reservoirs, irrigation systems, rice fields). year, year, st Basic biological features Reproduction above 23°C, maturing at 7 months, breeding capacity of up to 1500 eggs, tolerant of 4-35°C (best growth: 25-30°C), medium salinity tolerance (12 psu), lower dissolved oxygen lethal limit of 0.5 mg/L), max length: 35 cm TL, life span: 4-5 years, omnivorous-polytrophic. Reproduction >15°C, breeding capacity of up to 450 eggs, life span: 3-6 years, breeding before 1 tolerant of 1-35°C (best growth: 22-30), medium salinity tolerance (up to 12 psu), lower dissolved oxygen lethal limit of 1.0 mg/L), max length: 15 cm omnivorous- TL, burrowing ability, polytrophic. Max size up to 7 cm, breeding capacity up to 300 eggs, kept in 20-26°C aquaria (apparently wider tolerance in nature), moderate salinity tolerance, blue-color mutation, burrowing ability, omnivorous-polytrophic. Reproduction >10°C, temperature tolerant ≤ 35ºC (best growth: 22-30ºC), breeding capacity over 600 r-selected, eggs, rapid growth, life span: 4 years, max length: 15 cm TL, tolerant of brackish water (12 psu) and adverse environmental conditions ( e.g. lower dissolved oxygen lethal limit of 0.4 mg/L), burrowing ability, omnivorous-polytrophic. state origin States Native Florida Guinea Eastern Australia Northern S.E United Australia & Papua New Papua PCA CXD PCC Abbreviation name crayfish crayfish Redclaw CXQ Common Florida blue Red swamp 1868 Clark, 1936 Yabby Faxon, 1884 Faxon, Girard, 1852 von Martens, aquarium market with their basic biological features, habitat preferences and impacts. List of non-indigenous freshwater crayfish species in the Greek aquarium alleni clarkii Cherax Cherax Species Authority destructor Procambarus Procambarus quardicarinatus Table 1. Table

13 Enemy at the gates: introduction potential of non-indigenous freshwater crayfish in Greece via the aquarium trade [ 35 , 36 ] [ 33 , 34 ] [ 28 , 29 ] Source [ 9 , 30 - 32 ] Documented/ possible impacts Unknown but possible carrier of the ‘plague’ Invasive. Impacts in the area of origin, (aggressiveness, dominance and range expansion over other native crayfish species, intermediate host of parasites) and possible carrier of the ‘plague’. Unknown but possible carrier of the ‘plague’ Unknown. Habitat preferences Lentic (lakes, springs). Primarily lentic (swamps, ditches, lakes, ponds, oxbow lakes and sluggish streams). Primarily lentic (swamps, ponds, sluggish streams, rivers, lakes, reservoirs and canal banks). Lotic-Lentic (slow flowing, still waters). Basic biological features Short-lived (18 months), small-sized Short-lived (up to 4 cm), orange-color mutation in aquarium market, temperature tolerance of 10-26°C, breeding capacity up to 60 eggs omnivorous-polytrophic. Conservation status according to IUCN: Endangered. Short-lived (2-3 years), small-sized (up Short-lived to 3.8 cm), temperature preference of 18-24°C, breeding capacity of 30-40 omnivorous- eggs, burrowing ability, polytrophic. (2 years), small-sized (up Short-lived to 4 cm), temperature tolerance of 10-25°C, breeding capacity up to 120 eggs, omnivorous-polytrophic. Tolerate 18-29°C, persist where Tolerate habitat modification has been severe, omnivorous- burrowing ability, polytrophic, life-span: 5-7 years. New origin Native Papua, Papua, Guinea Southern US states CXP CAP Mexico CAS CAM Mexico Abbreviation name crayfish crayfish Common Cajun dwarf Dwarf orange Dwarf crayfish Zebra crayfish 1943 1857 List of non-indigenous freshwater crayfish species in the Greek aquarium market with their basic biological features, habita t preferences and impacts. Villalobos Saussure, Lukhaup & Faxon, 1884 Faxon, Herbert, 2008 Table 1. Table Species Authority shufeldtii Cambarellus Cambarellus Cambarellus montezumae patzcuarensis Cherax peknyi continued

14 I. Papavlasopoulou et al.

Figure 1. FI-ISK invasiveness score for selected aquarium NICS (CXQ, CXD and PCC), established NICS (PFL) and ICS (APT, ASA and ASL) in Greece (current study) and Italy (data from Tricarico et al. [9]). Solid line indicates the threshold level of ‘high risk’ species. APT: Austropotamobius torrentium, ASA: Astacus astacus, ASL: Astacus leptodactylus, CXQ: Cherax quadricarinatus, CXD: Cherax destructor, PFL: Pacifastacus leniusculus, PCC: Procambarus clarkii. various human-mediated vectors of introduction may be transmitted to humans. Finally, P. clarkii is able to threaten existing ICS populations in these countries. accumulate cyanobacterial toxins [19] and subsequently Such vectors include legal or illegal stocking in natural transfer them to their predators as well as to humans. water bodies, aquaculture, live food trade, aquarium Populations of P. clarkii are widespread in Europe, and pond trade and, to a lesser extent, biological supply particularly in Spain, Italy and southern France, which trade for experimental purposes and live bait [11]. The have similar climatic conditions to Greece. P. clarkii is main threats assessed for ICS in Greece in this study also present in various climatic zones (from Israel to are summarised in Table 2. Belgium), including several insular populations [2,14]. Although NICS introduced since the mid-19th Similarly, C. destructor is thriving in Spain and an century up to 1975 were introduced primarily to established population was recently found in central re-stock overfished European crayfish populations and Italy [2,3,20]. Finally, the tropical C. quardicarinatus for aquaculture, many recently introduced NICS were has recently established a self-sustaining population in brought into Europe via the aquarium trade since the thermal hot springs in Slovenia [21]. The introduction 1980s [2]. Of all the NICS assessed in our survey, of C. quardicarinatus could also happen in warmer P. clarkii is listed among the hundred worst invasive parts of southern Greece, since this species tolerates species in Europe and among the top 27 species temperatures down to 4°C [22]. Currently, there are no introduced into Europe for aquaculture and related available data on introduction/establishment of the rest activities [12,13]. Although fishing ofP. clarkii constitutes of the NICS surveyed during the present work in the at least 50% of the European ICS fisheries production European aquatic ecosystems. [3], there are examples of pronounced adverse effects The aquarium trade of NICS is largely uncontrolled of this species on native ecosystems in diverse around the globe. As a result, the risk of further locations around the world: negative impacts in littoral freshwater crayfish introductions in European and semi-terrestrial marsh ecosystems in southern waters is considerable. Based on recent studies of Spain [14]; destruction of reed-beds and intensive ornamental fish [23] and crayfish 24 [ ] species, there is predation on native fish species in Lake Naivasha in a clear relationship between the frequency of species Kenya [15]; decreased rice production in Portugal [16]; occurrence and size in the aquarium trade industry and and damages to river banks and agricultural fields due the likelihood of introduction/establishment into the wild. to its burrowing activity in the USA [17]. Additionally, Moreover, trade laws of the single European market P. clarkii is one of the most important vector of crayfish (i.e. free movement of goods and services), need to ‘plague’, carrying the pathogen (Aphanomyces astaci consider the potential risks from aquarium trade. The most Schikora) as a chronic infection [18] and may also be noteworthy example is the largely unregulated German an intermediate host for helminth parasites which can aquarium trade market (regular and internet-based)

15 Enemy at the gates: introduction potential of non-indigenous freshwater crayfish in Greece via the aquarium trade

Cumulative Threats ASA APT ASL Justification/Comments Score NICS in aquarium trade/Favourable climatic conditions. NICS 3 3 3 9 One established population of PFL neighbouring to ASA and APT populations. All ICS susceptible to plague. Massive mortalities and Crayfish plague 3 3 3 9 suspected incidents in the past. Increased during the last decades for all species. Fragmentation 2/3 3 2/3 7-9 More severe due to the already geographically isolated populations and augmented by anthropogenic impacts.

Serious problem by agricultural intensification. Toxicants 2/3 2/3 2/3 6-9 Irresponsible use and deposit practises.

Expected to have a varied but increasingly important Climate change 2 3 1/2 6-7 impact in inland waters. Directly related to the adaptability of each species (reduced for APT). Significant and on-going (e.g. dams, public and Habitat alterations 2 2/3 1/2 5-7 hydraulic works). Water abstraction significant in many lowland areas/ Water abstraction and 2 2 0/1 4-5 lakes. However, ICS populations are currently water level reduction constrained in less lowland and populated areas. Poor or medium quality of many lakes primarily affecting Eutrophication 2 1/2 1 4-5 important ASA populations in the past. APT populations mainly in pristine brooks not close to agricultural fields.

Land-use 2 1 1 4 Moderate for lowland ASA populations.

Diminishing populations of top predators (e.g. eel, trout, European catfish, pike perch). Birds and other higher Predators 1 1 1 3 terrestrial or aquatic may be in some cases more important predators. Low intensity by recreational fishermen being disputably harmful, except in slow growth populations in high Exploitation 1 0/1 0 1-2 altitudes. Crayfishing and cooking tradition in very limited places. Data completely missing, except for commensal Other diseases ? ? ? ? branchiobdellids. 1.75-2.08 Values in parentheses refer to the mean range of the Mean range of threat level 2.00-2.18 1.90-2.27 1.36-1.81 (5.27-6.27) cumulative scores. The ASL population is unique to the country. Accordingly, it could be handled as a threatened population, after a IUCN conservation status VU VU Not listed thorough assessment, given the transboundary nature of its habitat.

EU Habitats EU Habitats EU Habitats Directive 92/43/EEC and NATURE 2000 Directive Directive Protection frameworks Not listed framework are only marginally effective (e.g. no SPAs 92/43/EEC 92/43/EEC - Species Protection Areas - have been designated for (Appendix V) (Appendix II) APT). Consolidated national legislation is urgently needed for the protection of ICS and their habitats. The 708/2007 (EC) Directive does not directly apply to the aquarium trade; however it introduces the ‘white list’ approach for the importation of species and provides Royal Decree 142/71, FEK 49A/71 (open season from the responsibility to the Member States to take the 15th of February to 15th of May and minimum size of 10 appropriate measures to protect biodiversity threatened cm TL) by the movement of aquatic animals for aquaculture No 147703/4.7.2002 Ministerial Act for import permission purposes. Greece may not fulfil the EU Water Directive Legislation for alien species via a central commission (2000/60/EC) goals of ‘good ecological status’ and 708/2007 (EC) Directive for the use of alien and locally ‘good chemical status’ of surface and ground waters absent species in aquaculture by the year 2015. Recent environmental-ecological NATURE 2000 studies on the larger lakes of the country showed that EU Water Directive (2000/60/EC). most of them are currently disturbed, falling into the ‘poor’, ‘bad’ or ‘moderate’ water quality classes based on pH, chlorophyll-α concentration, Secchi depth, total phosphorus, high proportion of cyanobacteria in phytoplankton communities and limited macrophyte coverage [37].

Table 2. Quantitative scoring of the significance of the main threats to ICS in Greece and available protection frameworks; 0=none, 1=low, 2=medium, 3=high.

16 I. Papavlasopoulou et al.

of live ornamental freshwater crayfish with 120 NICS of the main import channels for NICS, banning the available in stores, including 105 species considered to import of highly invasive NICS (e.g., P. clarkii and be high-risk vectors of crayfish ‘plague’ [24]. C. destructor), and banning translocations of invasive Our results suggest that the number of NIFCS ICS after a thorough assessment within the context of available in the Greek domestic market is relatively the ‘white list’ approach of the 708/2007 (EC) Directive low compared both to other animal taxa, and to [3]; (b) setting up a contingency plan with mechanisms other European countries (e.g., Germany and Czech to promote rapid responses in the event of NICS and Republic) This trend may be due to the low popularity crayfish ‘plague’ introductions in Europe; and (c) strict of freshwater crayfish among aquarium hobbyists enforcement of legislation. Moreover, several additional and their higher prices compared to many popular initiatives could support the biodiversity of freshwater aquarium fish (e.g., €5-50 for P. clarkii, C. destructor and aquatic species in Greece, including a framework to C. quadricarinatus and about €15 for Cambarellus monitor and control of the signal crayfish population species). However, given the absence of public in northern Greece, the protection of ICS populations education and sensitization of local communities, NICS and their habitats through the designation of SPAs as introductions still constitute a considerable risk to ICS in well as re-introduction programs, the enhancement Greece via deliberate or accidental releases. Accordingly, of public education on the risk of NICS introductions efforts to protect the native freshwater biodiversity of (e.g., through responsible aquarium management) Greek freshwater systems should concentrate on several and research support on applied invasion biology and management initiatives, including (a) the identification management.

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